Differential Induction of Topoisomerase I-DNA Cleavage Complexes by the Indenoisoquinoline MJ-III-65 (NSC 706744) and Camptothecin: Base Sequence Analysis and Activity against Camptothecin-Resistant Topoisomerases I

Cancer Research

Volumn 63, Issue 21, 2003, Pages 7428-7435

  Antony, Smitha ^a   Jayaraman, Muthusamy ^b   Laco, Gary ^a   Kohlhagen, Glenda ^a   Kohn, Kurt W ^a   Cushman, Mark ^b   Pommier, Yves ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTINEOPLASTIC AGENT; CAMPTOTHECIN; CAMPTOTHECIN DERIVATIVE; CYTOSINE; DNA TOPOISOMERASE; DNA TOPOISOMERASE INHIBITOR; GUANINE; INDENE DERIVATIVE; ISOQUINOLINE DERIVATIVE; LACTONE; NSC 706744; THYMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; DRUG INACTIVATION; DRUG SENSITIVITY; DRUG TARGETING; HUMAN; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RING OPENING; SEQUENCE ANALYSIS; SIDE EFFECT; TUMOR RESISTANCE; VACCINIA VIRUS;

ANIMALS; CAMPTOTHECIN; DNA; DNA TOPOISOMERASES, TYPE I; ENZYME INHIBITORS; HUMANS; INDENES; ISOQUINOLINES; OLIGONUCLEOTIDES; SUBSTRATE SPECIFICITY; VACCINIA;

EID: 0242610818     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Pommier, Y., Pourquier, P., Urasaki, Y., Wu, J., and Laco, G. Topoisomerase I inhibitors: selectivity and cellular resistance. Drug Resistance Update. 2: 307-318, 1999.
2. Guichard, S. M., and Danks, M. K. Topoisomerase enzymes as drug targets. Curr. Opin. Oncol., 11: 482-489, 1999.
3. Liu, L. F., Desai, S. D., Li, T. K., Mao, Y., Sun, M., and Sim, S. P. Mechanism of action of camptothecin, Ann N. Y. Acad. Sci., 922: 1-10, 2000.
4. Meng, L-H., Liao, Z-H., and Pommier, Y. Non-camptothecin DNA topoisomerase I inhibitors in cancer chemotherapy. Curr. Top. Med. Chem., 3: 305-320, 2003.
5. Pommier, Y. Review on mechanisms of action of topoisomerase I poisons. http://discover.nci.nih.gov/pommier/topo1.htm, 2003.
6. Jaxel, C., Kohn, K. W., Wani, M. C., Wall, M. E., and Pommier, Y. Structure-activity study of the actions of camptothecin derivatives on mammalian topoisomerase I: evidence for a specific receptor site and a relation to antitumor activity. Cancer Res., 49: 1465-1469, 1989.
7. Covey, J. M., Jaxel, C., Kohn, K. W., and Pommier, Y. Protein-linked DNA strand breaks induced in Mammalian cells by camptothecin, an inhibitor of topoisomerase I. Cancer Res., 49: 5016-5022, 1989.
8. Pommier, Y., Fesen, M. R., and Goldwasser, F. Topoisomerase II inhibitors: the epipodophyllotoxins, m-AMSA, and the ellipticine derivatives. In: B. A. Chabner and D. L. Longo (eds.), Cancer Chemotherapy and Biotherapy: Principles and Practice, Ed. 2, pp. 435-461. Philadelphia: Lippincott-Raven, 1996.
9. Paull, K. D., Shoemaker, R. H., Hodes, L., Monks, A., Scudiero, D. A., Rubinstein, L., Plowman, J., and Boyd, M. Display and analysis of patterns of differential activity of drugs against human tumor cell lines: development of a mean graph and COMPARE algorithm. J. Natl. Cancer Inst. (Bethesda), 81: 1088-1092, 1989.
10. Paull, K. D., Hamel, E., and Malpeis, L. Prediction of biochemical mechanism of action from the in vitro antitumor screen of the National Cancer Institute. In: W. O. Foye (ed.), Cancer Chemotherapeutic Agents, pp. 8-45. Washington, DC: ACS, 1995.
11. Boyd, M. R., and Paull, K. D. Some practical considerations and applications of the National Cancer Institute in vitro anticancer drug discovery screen. Drug Dev. Res., 34: 91-109. 1995.
12. Kohlhagen, G., Paull, K. D., Cushman, M., Nagafuji, P., and Pommier, Y. Protein-linked DNA strand breaks induced by NSC 314622, a novel noncamptothecin topoisomerase I poison. Mol. Pharmcol. 54: 50-58, 1998.
13. Strumberg, D., Pommier, Y., Paull, K., Jayaraman, M., Nagafuji, P., and Cushman, M. Synthesis of cytotoxic indenoisoquinoline topoisomerase I poisons. J. Med. Chem., 42: 446-457, 1999.
14. Cushman, M., Jayaraman, M., Vroman, J. A., Fukunaga, A. K., Fox, B. M., Kohlhagen, G., Strumberg, D., and Pommier, Y. Synthesis of new indeno[1,2-c]isoquinolines: cytotoxic non-camptothecin topoisomerase I inhibitors. J. Med. Chem., 43: 3688-3698, 2000.
15. Jayaraman, M., Fox, B. M., Hollingshead, M., Kohlhagen, G., Pommier, Y., and Cushman, M. Synthesis of new dihydroindeno[1,2-c]isoquinoline and indenoisoquinolinium chloride topoisomerase I inhibitors having high in vivo anticancer activity in the hollow fiber animal model. J. Med. Chem., 45: 242-249. 2002.
16. Fujimori, A., Harker, W. G., Kohlhagen, G., Hoki, Y., and Pommier, Y. Mutation at the catalytic site of topoisomerase I in CEM/C2. a human leukemia cell resistant to camptothecin. Cancer Res., 55: 1339-1346, 1995.
17. Urasaki, Y., Takebayashi, Y., and Pommier, Y. Activity of a novel camptothecin analogue, homocamptothecin, in camptothecin-resistant cell lines with topoisomerase I alterations. Cancer Res., 60: 6577-6580. 2000,
18. Urasaki, Y., Laco, G., Takebayashi, Y., Bailly, C., Kohlhagen, G., and Pommier, Y. Use of camptothecin-resistant mammalian cell lines to evaluate the role of topoisomerase I in the antiproliferative activity of the indolocarbazole, NB-506, and its topoisomerase I binding site, Cancer Res., 61: 504-508, 2001.
19. Urasaki, Y., Laco, G. S., Pourquier, P., Takebayashi, Y., Kohlhagen, G., Gioffre, C., Zhang, H., Chatterjee, D., Pantazis, P., and Pommier, Y. Characterization of a novel topoisomerase I mutation from a camptothecin-resistant human prostate cancer cell line. Cancer Res., 61: 1964-1969, 2001.
20. Laco, G. S., Collins, J. R., Luke, B. T., Kroth, H., Sayer, J. M., Jerina, D. M., and Pommier, Y. Human topoisomerase I inhibition: docking camptothecin and derivatives into a structure-based active site model. Biochemistry. 41: 1428-1435, 2002.
21. Pourquier, P., Pilon, A., Kohlhagen, G., Mazumder, A., Sharma, A., and Pommier, Y. Trapping of mammalian topoisomerase I and recombinations induced by damaged DNA containing nicks or gaps: importance of DNA end phosphorylation and camptothecin effects. J. Biol. Chem., 272: 26441-26447, 1997.
22. Pourquier, P., Takebayashi, Y., Urasaki, Y., Gioffre, C., Kohlhagen, G., and Pommier, Y. Induction of topoisomerase I cleavage complexes by I-β-D-arabinofuranosylcytosine (Ara-C) in vitro and in ara-C-treated cells. Proc. Natl. Acad. Sci. USA, 97: 1885-1890, 2000.
23. Zhelkovsky, A. M., Moore, C. L., Rattner, J. B., Hendzel, M. J., Furbee, C. S., Muller, M. T., and Bazett-Jones, D. P. Overexpression of human DNA topoisomerase I in insect cells using a baculovirus vector, Protein Expr. Purif., 5: 364-370, 1994.
24. Redinbo, M. R., Stewart, L., Kuhn, P., Champoux, J. J., and Hol, W. G. J. Crystal structure of human topoisomerase I in covalent and noncovalent complexes with DNA. Science (Wash. DC), 279: 1504-1513, 1998.
25. Stewart, L., Redinbo, M. R., Qiu, X., Hol, W. G. J., and Champoux, J. J. A model for the mechanism of human topoisomerase 1. Science (Wash. DC), 279: 1534-1541, 1998.
26. Shuman, S., and Moss, B. Characterization of vaccinia virus DNA topoisomerase I expressed in Escherichia coli, J. Biol. Chem., 263: 16401-16407, 1988.
27. Pourquier, P., Kohlhagen, G., Ueng, L-M., and Pommier, Y. Topoisomerase I and II activity assays. In: R. Brown and U. Böger-Brown (eds.), Methods in Molecular Medicine: Cytototoxic Drug Resistance Mechanisms. Vol. 28, pp. 95-110. Totowa, NJ: Humana Press, 1999.
28. Petersen, B. O., Wittschieben, J., and Shuman, S. Mutations within a conserved region of vaccinia topoisomerase affect the DNA cleavage-religation equilibrium. J. Mol. Biol., 263: 181-195, 1996.
29. Hsiang, Y. H., Hertzberg, R., Hecht, S., and Liu. L. F. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem., 260: 14873-14878, 1985.
30. Kjeldsen, E., Svejstrup, J. Q., Gromova, I. I., Alsner, J., and Westergaard, O. Camptothecin inhibits both the cleavage and religation reactions of eukaryotic DNA topoisomerase I. J. Mol. Biol., 228: 1025-1030, 1992.
31. Tanizawa, A., Kohn, K. W., Kohlhagen, G., Leteurtre, F., and Pommier, Y. Differential stabilization of eukaryotic DNA topoisomerase I cleavable complexes by camptothecin derivatives. Biochemistry, 34: 7200-7206, 1995.
32. Porter, S. E., and Champoux, J. J. Mapping in vivo topoisomerase I sites on simian virus 40 DNA: asymmetric distribution of sites on replicating molecules. Mol. Cell. Biol., 9: 541-550, 1989.
33. Jaxel, C., Kohn, K. W., and Pommier, Y. Topoisomerase I interaction with SV40 DNA in the presence and absence of camptothecin. Nucleic Acids Res., 16: 11157-11170, 1988.
34. Valenti, M., Nieves-Neira, W., Kohlhagen, G., Kohn, K. W., Wall, M. E., Wani, M. C., and Pommier, Y. Novel 7-alkyl methylenedioxycamptothecin derivatives exhibit increased cytotoxicity and induce persistent cleavable complexes both with purified mammalian topoisomerase I and in human colon carcinoma SW620 cells. Mol. Pharmacol., 52: 82-87, 1997.
35. Bonven, B. J., Gocke, E., and Westergaard, O. A high affinity topoisomerase I binding sequence is clustered at DNase I hypersensitive sites in Tetrahymena R-chromatin. Cell, 41: 541-551, 1985.
36. Staker, B. L., Hjerrild, K., Feese, M. D., Behnke, C. A., Burgin, A. B., Jr., and Stewart, L. The mechanism of topoisomemse I poisoning by a camptothecin analog, Proc. Natl. Acad. Sci. USA. 99: 15387-15392, 2002.
37. Jaxel, C., Capranico, G., Kerrigan, D., Kohn, K. W., and Pommier, Y. Effect of local DNA sequence on topoisomerase I cleavage in the presence or absence of camptothecin. J. Biol. Chem., 266: 20418-20423, 1991.
38. Thomsen, B., Mollerup, S., Bonven, B. J., Frank, R., Blocker, H., Nielsen, O. F., and Westergaard, O. Sequence specificity of DNA topoisomerase I in the presence and absence of camptothecin. EMBO J. 6: 1817-1823, 1987.
39. Shuman, S. Site-specific DNA cleavage by Vaccinia virus DNA topoisomerase I. Role of nucleotide sequence and DNA secondary structure. J. Biol. Chem., 266: 1796-1803, 1991.
40. Cushman, M., and Cheng, L. Stereoselective oxidation by thionyl chloride leading to the indeno[1,2-c]isoquinoline system. J. Org. Chem., 43: 3781-3783, 1978.
41. Jayaraman, M., Fanwick, P. E., and Cushman, M. Novel oxidative transformation of indenoisoquinolines to isoquinoline-3-spiro-3′ -phthalides in the presence of osmium tetraoxide and 4-methylmorpholine N-oxide. J. Org. Chem., 63: 5736-5737, 1998.
42. Fox, B. M., Xiao, X., Antony, S., Kohlhagen, G., Pommier, Y., Staker, B. L., Stewart, L., and Cushman, M. Design, synthesis, and biological evaluation of cytotoxic 11-alkenylindenoisoquinoline-camptothecin hybrids. J. Med. Chem., 46: 3275-3282, 2003.
43. Haaz, M. C., Rivory, L. P., Riche, C., and Robert, J. The transformation of irinotecan (CPT-11) to its active metabolite SN-38 by human liver microsomes. Differential hydrolysis for the lactone and carboxylate forms. Naunyn Schmiedebergs Arch. Pharmacol., 356: 257-262, 1997.
44. Morton, C. L., Wadkins, R. M., Danks, M. K., and Potter, P. M. The anticancer prodrug CPT-11 is a potent inhibitor of acetylcholinesterase but is rapidly catalyzed to SN-38 by butyrylcholinesterase. Cancer Res., 59: 1458-1463, 1999.
45. Hertzberg, R. P., Caranfa, M. J., Holden, K. G., Jakas, D. R., Gallagher, G., Mattern, M. R., Mong, S. M., Bartus, J. O., Johnson, R. K., and Kingsbury, W. D. Modification of the hydroxy lactone ring of camptothecin: inhibition of mammalian topoisomerase I and biological activity. J. Med. Chem., 32: 715-720, 1989.
46. Lesueur-Ginot, L., Demarquay, D., Kiss, R., Kasprzyk, P. G., Dassonneville, L., Bailly, C., Camara, J., Lavergne, O., and Bigg, D. C. Homocamptothecin, an E-ring modified camptothecin with enhanced lactone stability, retains topoisomerase I-targeted activity and antitumor properties. Cancer Res., 59: 2939-2943, 1999.
47. Burke, T. G., and Mi, Z., M. The structural basis of camptothecin interactions with human serum albumin: impact on drug stability. J. Med. Chem., 37: 40-46, 1994.
48. Knab, A. M., Fertala, J., and Bjornsti, M. A. Mechanisms of camptothecin resistance in yeast DNA topoisomerase I mutants. J. Biol. Chem., 268: 22322-22330, 1993.
49. Fiorani, P., Amatruda, J. F., Silvestri, A., Butler, R. H., Bjornsti, M. A., and Benedetti, P. Domain interactions affecting human DNA topoisomerase I catalysis and camptothecin sensitivity. Mol. Pharmacol., 56: 1105-1115, 1999.
50. Fertala, J., Vance, J. R., Pourquier, P., Pommier, Y., and Bjomsti, M-A. Substitution of Asn-726 in the active site of yeast DNA topoisomerase I define a novel mechanisms of stabilizing the covalent enzyme-DNA intermediate. J. Biol. Chem., 275: 15246-15253, 2000.
51. Champoux, J. J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem., 70: 369-413, 2001.